Abstract
Physiological and biochemical studies have provided evidence that mechanical strain (touch)-induced modifications in plant growth and development may be due to ethylene. In order to better understand the involvement of ethylene in touch-induced responses, we identified and characterized an Arabidopsis cDNA (ACS6) encoding 1-aminocyclopropane-1-carboxylic acid (ACC) synthase which is an important regulatory enzyme in the ethylene biosynthetic pathway. Northern analysis showed that ACS6 was induced by touch in the leaves of 3-week old light-grown plants within 5 min and reached maximum transcription at 15 min. ACC, which is the product of ACC synthase and the immediate precursor to ethylene, exhibited a dramatic rise between 15 and 30 min after touch stimulation. Experiments with multiple touch treatments showed that a saturation in gene expression was obtained with one touch treatment and subsequent touch stimulations were progressively less effective in promoting ACS6 expression. Additional characterization of ACS6 gene expression indicated that the gene is also induced by wounding, and by treatment with LiCl, NaCl, CuCl2, auxin, cycloheximide (CHX), aminooxyacetic acid (AOA) and ethylene. ACC levels were also increased in response to each of these treatments with the exception of CHX and AOA which resulted in a decrease and no effect, respectively. Our results show that ACS6 is rapidly turned on in response to touch which is followed by an increase in ACC which is the immediate precursor to ethylene, thereby providing evidence that it is responsible for touch-inducible ethylene production in light-grown Arabidopsis plants. The identification and characterization of ACS6 now provides us with a tool to better understand the involvement of ethylene produced in response to external stimuli as well as during plant growth and development.
Similar content being viewed by others
References
Abel S, Nguyen MD, Chow W, Theologis A: ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. J Biol Chem 270: 19093–19099 (1995).
Abeles FB, Morgan PW, Saltveit ME Jr: Ethylene in Plant Biology, 2nd ed. Academic Press, San Diego, CA (1992).
Botella JR, Arteca JM, Schlagnhaufer CD, Arteca RN, Phillips AT: Identification and characterization of a full-length cDNA encoding for an auxin-induced 1-aminocyclopropane-1-carboxylate synthase from etiolated mungbean hypocotyl segments and expression of its mRNA in response to indole-3-acetic acid. Plant Mol Biol 20: 425–436 (1992).
Botella JR, Arteca RN: Differential expression of two calmodulin genes in response to physical and chemical stimuli. Plant Mol Biol 24: 757–766 (1994).
Botella JR, Arteca RN, Frangos JA: A mechanical strain-induced ACC synthase gene. Proc Natl Acad Sci USA 92: 1595–1598 (1995).
Botella JR, Arteca JM, Somodevilla M, Arteca RN: Calcium-dependent protein kinase gene expression in response to physical and chemical stimuli in mungbean. Plant Mol Biol 30: 1129–1137 (1996).
Braam J, Davis RW: Rain-wind-and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60: 357–364 (1990).
Braam J: Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc Natl Acad Sci USA 89: 3213–3216 (1992).
Church GM, Gilbert W: Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995 (1994).
Gawienowski MC, Szymanski D, Pereara IY, Zielinski RE: Calmodulin isoforms in Arabidopsis encoded by multiple divergent mRNAs. Plant Mol Biol 22: 215–225 (1993).
Huang PL, Parks JE, Rottmann WH, Theologis A: Two genes encoding 1-aminocyclopropane-1-carboxylate synthase in zucchini (Cucurbita pepo) are clustered and similar but differentially regulated. Proc Natl Acad Sci USA 88: 7021–7025 (1991).
Jaffe MJ, Forbes S: Thigmomorphogenesis: the effect of mechanical perturbation on plants. Plant Growth Regul 12: 313–324 (1993).
Jorgenson RA, Cuellar RE, Thompson WF: Modes and tempos in the evolution of nuclear encoded ribosomal RNA genes in legumes. Carnegie Inst Wash Yearb 81: 98–101 (1982).
Kende H: Ethylene biosynthesis. Annu Rev Plant Physiol Mol Biol 44: 283–307 (1993).
Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR: CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72: 427–441 (1993).
Knight MR, Campbell AK, Smith SM, Trewavas AJ: Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytosolic calcium. Nature 352: 524–526 (1991).
Liang X, Abel S, Keller JA, Shen NF, Theologis A: The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proc Natl Acad Sci USA 89: 11046–11050 (1992).
Liang X, Oono Y, Shen NF, Kohler C, Li K, Scolnik PA, Theologis A: Characterization of two members (ACS1 and ACS3) of the 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Gene 167: 17–24 (1995).
Liang X, Shen NF, Theologis A: Li+-regulated 1-aminocyclopropane-1-carboxylate synthase gene expression in Arabidopsis thaliana. Plant J 10: 1027–1036 (1996).
Ling V, Perera I, Zielinski RE: Primary structures of Arabidopsis calmodulin isoforms deduced from the sequences of cDNA clones. Plant Physiol 96: 1196–1202 (1991).
Mitchell CA: Recent advances in plant response to mechanical stress: theory and application. HortScience 31: 31–35 (1996).
Perera IY, Zielinski RE: Structure and expression of the Arabidopsis CAM-3 calmodulin gene. Plant Mol Biol 19: 649–664 (1992).
Pogson BJ, Downs CG, Davies KM, Morris SC: Nucleotide sequence of a cDNA clone encoding 1-aminocyclopropane-1-carboxylic acid synthase from broccoli. Plant Physiol 108: 857–858 (1995).
Rodrigues-Pousada RA, De Rycke R, Dedonder A, Van Caeneghem W, Engler G, Van Montagu M, Van der Straeten D: The Arabidopsis 1-aminocyclopropane-1-carboxylic acid synthase gene 1 is expressed during early development. Plant Cell 5: 897–911 (1993).
Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1989).
Selker JML, Steucek GL, Green PB: Biophysical mechanisms for morphogenetic progressions at the shoot apex. Dev Biol 153: 29–43 (1992).
Sistrunk ML, Antosiewicz DM, Purugganan MM, Braam J: Arabidopsis TCH3 encodes a novel Ca2+ binding protein and shows environmentally induced and tissue specific regulation. Plant Cell 6: 1553–1565 (1994).
Tsai DS, RN Arteca, JM Bachman, AT Phillips: Purification and characterization of 1-aminocyclopropane-1-carboxylic acid synthase from etiolated mung bean hypocotyls. Arch Biochem Biophys 264: 632–640 (1988).
Van Der Straeten D, Rodrigues-Pousada RA, Villarroel R, Hanley S, Goodman HM, Van Montagu M: Cloning, genetic mapping, and expression analysis of an Arabidopsis thaliana gene that encodes 1-aminocyclopropane-1-carboxylate synthase. Proc Natl Acad Sci USA 89: 9969–9973 (1992).
Wissocq J-C, Attias J, Thellier M: Exotic effects of lithium. In: Birch NJ (ed) Lithium and the Cell, pp. 7–34. Academic Press, NY (1991).
Xu W, Purugganan M, Polisensky D, Antosiewicz D, Fry S, Braam J: Arabidopsis TCH-4, regulated by hormones and the environment, encodes a xyloglucanase. Plant Cell 7: 1555–1567 (1995).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Arteca, J.M., Arteca, R.N. A multi-responsive gene encoding 1-aminocyclopropane-1- carboxylate synthase (ACS6) in mature Arabidopsis leaves. Plant Mol Biol 39, 209–219 (1999). https://doi.org/10.1023/A:1006177902093
Issue Date:
DOI: https://doi.org/10.1023/A:1006177902093